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Conflicting Functional Effects of Xylem Pit Structure Relate to the Growth-Longevity Trade-Off in a Conifer Species

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Conflicting Functional Effects of Xylem Pit Structure Relate to the Growth-Longevity Trade-Off in a Conifer Species Conflicting functional effects of xylem pit structure relate to the growth-longevity trade-off in a conifer species Beth Roskillya,1,2, Eric Keelingb, Sharon Hoodc, Arnaud Giuggiolad, and Anna Salaa aDivision of Biological Sciences, University of Montana, Missoula, MT 59812; bBiology Department, State University of New York, New Paltz, NY 12561; cFire, Fuel, and Smoke Science Program, Rocky Mountain Research Station, Forest Service, US Department of Agriculture, Missoula, MT 59808; and dPrivate address, 68128 Village-Neuf, France Edited by Douglas E. Soltis, University of Florida, Gainesville, FL, and approved May 23, 2019 (received for review January 18, 2019) Consistent with a ubiquitous life history trade-off, trees exhibit a imposed by individual traits and among multiple traits can therefore negative relationship between growth and longevity both among influence life history trade-offs. Multiple- and single-trait trade-offs and within species. However, the mechanistic basis of this life can be distinguished on the basis of the underlying selection regime. history trade-off is not well understood. In addition to resource Multiple-trait trade-offs arise when two or more fitness-enhancing allocation conflicts among multiple traits, functional conflicts arising traits are favored by selection but compete for a limiting resource from individual morphological traits may also contribute to life and/or share a genetic correlation (12). Examples include flower size history trade-offs. We hypothesized that conflicting functional versus number (13), offspring size versus number (14), and growth effects of xylem structural traits contribute to the growth-longevity versus defensive mechanisms in plants (15). On the other hand, trade-off in trees. We tested this hypothesis by examining the extent single-trait trade-offs arise due to opposing selection by different to which xylem morphological traits (i.e., wood density, tracheid selective agents, such as different environments or different com- diameters, and pit structure) relate to growth rates and longevity in ponents of fitness (12). Coat color in animals is an example of a two natural populations of the conifer species Pinus ponderosa.Hy- single-trait trade-off: darker or lighter coat color is favored to match draulic constraints arise as trees grow larger and xylem anatomical different seasonal background environments with dramatic conse- traits adjust to compensate. We disentangled the effects of size quences on fitness (16). Although trade-offs among multiple traits through ontogeny in individual trees and growth rates among trees have been the focus of many life history studies, the contribution of on xylem traits by sampling each tree at multiple trunk diameters. We single-trait trade-offs warrants further attention. found that the oldest trees had slower lifetime growth rates com- In trees, competing functional demands on stem xylem mor- pared with younger trees in the studied populations, indicating a phological traits may lead to a growth-longevity trade-off. Stem growth-longevity trade-off. We further provide evidence that a single xylem performs several physiological functions critical to tree xylem trait, pit structure, with conflicting effects on xylem function growth and survival, including efficient water transport, embolism (hydraulic safety and efficiency) relates to the growth-longevity resistance, and mechanical safety (17, 18). Trees require water to trade-off in a conifer species. This study highlights that, in addition to trade-offs among multiple traits, functional constraints based on individual morphological traits like that of pit structure provide mech- Significance anistic insight into how and when life history trade-offs arise. Understanding life history trade-offs is important because they life history | plant hydraulics | xylem anatomy | present limits to adaptation in organisms. Life history trade- growth-longevity trade-off | pit structure offs are usually thought to result from resource allocation conflicts among multiple traits, but functional constraints based on individual morphological traits can also contribute. ife history trade-offs are important because they present We show that a fundamental life history trade-off between adaptive constraints on the most proximal components of L growth and longevity in a conifer species is related to a single fitness (1). A ubiquitous life history trade-off across organisms is morphological trait in the xylem that has conflicting functional that between growth and life span; organisms that grow slowly tend effects. Our results demonstrate that, in addition to resource to live longer than those with faster growth, indicating that rapid allocation trade-offs among multiple traits, functional con- growth is associated with reduced longevity (2). Consistent with the straints based on individual morphological traits provide growth-longevity trade-off, slow early growth in trees has been as- mechanistic insight into how and when life history trade- sociated with longer life spans in several species (3–9). However, in offs arise. trees, fast growth rates and large size also provide fitness benefits via increased competitive ability, faster time to reproduction, and in- Author contributions: B.R., E.K., A.G., and A.S. designed research; B.R., E.K., and A.G. creased chances of early survival (10). Yet, selection for fast growth performed research; B.R., S.H., and A.S. contributed new reagents/analytic tools; B.R., rates early in life can conflict with selection for slow growth at ma- E.K., S.H., and A.S. analyzed data; and B.R. and A.S. wrote the paper. ture stages, as shown in adult Pinus ponderosa during a bark beetle The authors declare no conflict of interest. outbreak (11). Although resource allocation conflicts have been This article is a PNAS Direct Submission. shown to drive life history trade-offs (2), we know less about how Published under the PNAS license. morphological traits contribute. Nonetheless, understanding the Data deposition: Data reported in this paper have been publicly archived in the Dryad functional trade-offs of specific morphological traits can enhance our digital repository, https://doi.org/10.5061/dryad.31ns53c. ability to predict when and how life history trade-offs arise. See Commentary on page 14794. Life history trade-offs are usually interpreted as trade-offs that 1To whom correspondence may be addressed. Email: [email protected]. result from resource allocation conflicts among multiple traits 2Present address: Department of Forest and Conservation Sciences, University of British that enhance fitness (12). Indeed, life history traits such as Columbia, Vancouver, BC, Canada V6T 1Z4. growth, reproduction, and survival require large investments This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. in available resources and depend on a complex network of 1073/pnas.1900734116/-/DCSupplemental. interrelated morphological and functional traits. Constraints Published online June 17, 2019. 15282–15287 | PNAS | July 23, 2019 | vol. 116 | no. 30 www.pnas.org/cgi/doi/10.1073/pnas.1900734116 Downloaded by guest on September 29, 2021 assimilatecarbonandtomaintaincellularturgortopromotetissue C. Lawson var. ponderosa C. Lawson). We tested this hypothesis growth and function; therefore, water transport efficiency is posi- by examining the extent to which xylem morphological traits (i.e., tively related to growth rate (19–22). Embolism resistance, or the wood density, tracheid diameters, and pit structure) relate to SEE COMMENTARY ability to tolerate high tensions in the xylem without hydraulic growth rates and longevity in two natural populations. By fo- failure, allows for the maintenance of water transport and survival cusing on a single conifer species we were able to examine the during drought (23, 24). Mechanical safety provides protection role of each xylem trait in growth and longevity while minimizing against physical damage, such as that caused by wind, pests, or the types of variation in xylem structure observed among species. pathogens, and cellular implosion under high xylem tension, and Hydraulic constraints arise as trees grow taller, with xylem ana- thus it is also related to survival (18, 25). tomical traits expected to adjust to compensate for these con- When multiple critical functions depend on the same xylem straints (32, 33). We therefore disentangled the effects of size morphological traits, functional conflicts can arise with impor- through ontogeny in individual trees and growth rates among tant consequences for tree growth and survival. This pattern may trees on xylem traits by retrospectively sampling each tree at be more prevalent in conifers compared with angiosperm trees multiple trunk diameters. We found that the oldest trees had due to fundamental differences in xylem structure. In angiosperms, slower lifetime growth rates compared with younger trees in the specialized cell types perform distinct functions. For example, populations that we studied, indicating a growth-longevity trade- vessels transport water while fibers provide biomechanical support. off. Furthermore, we provide evidence that a single xylem trait, The physical separation between biomechanical support and water pit structure, relates to the growth-longevity trade-off in a conifer transport in angiosperms allows vessels to reach large dimensions, species due to its conflicting effects on hydraulic safety and thus decreasing resistance to water flow
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